Solenn Stoeckel’s research while affiliated with Institut Français de Recherche pour l'Exploitation de la Mer and other places

Sexual to asexual transition is described as a process whereby asexual lineages emerge within sexual species. This phenomenon gives rise to many questions about the maintenance of sexual reproduction and the evolution of asexuality in these organisms. The poplar rust fungus Melampsora larici-populina has a complex life cycle, which is typical of rust fungi (Pucciniales). It alternates between a sexual reproduction phase on larch trees (Larix spp.) and rounds of asexual multiplication on poplar trees (Populus spp.). This alternation between sexual and asexual reproduction shows some similarities with the cyclical parthenogenesis observed in aphids and daphnia. This study challenges the classic understanding of the M. larici-populina life cycle. Our results demonstrate the existence of many distinct lineages that reproduce asexually through the years, skipping the sexual phase. We conducted a comprehensive population genetic analysis, utilizing 21 microsatellite markers and data from over 2000 individuals gathered over an extended period of time from various locations in France. A clustering analysis identified a group of multilocus lineages that displayed all hallmarks of the genetic consequences of asexual reproduction, including highly negative and large variance among loci of the inbreeding coefficient (FIS). This indirect evidence for asexual reproduction was confirmed by the direct observation of these asexual lineages being repeatedly sampled over the years, confirming the findings of variations in M. larici-populina life cycle with lineages that bypass the mandatory sexual phase. While sexual lineages are predominant throughout France, asexual lineages are more prevalent in the south of the country, due to possible environmental or ecological factors that allow the overwintering of asexual forms. The discovery of variations in the life cycle in this species offers insights into the evolution from sexual to asexual reproduction encountered in many pathogen species. It could serve as a model organism for studying the transition from sexual to asexual reproductive mode.

Temporal population genetic studies have investigated evolutionary processes, but few have characterized reproductive system variation. Yet, temporal sampling may improve our understanding of reproductive system evolution through the assessment of the relative rates of selfing, outcrossing, and clonality. In this study, we focused on the monoicous, haploid‐diploid freshwater red alga Batrachospermum gelatinosum . This species has a perennial, microscopic diploid phase (chantransia) that produces an ephemeral, macroscopic haploid phase (gametophyte). Recent work focusing on single‐time point genotyping suggested high rates of intragametophytic selfing, although there was variation among sites. We expand on this work by genotyping 191 gametophytes sampled from four sites that had reproductive system variation based on single‐snapshot genotyping. For this study, we sampled at multiple time points within and among years. Results from intra‐annual data suggested shifts in gametophytic genotypes throughout the season. We hypothesize that this pattern is likely due to the seasonality of the life cycle and the timing of meiosis among the chantransia. Interannual patterns were characterized by consistent genotypic and genetic composition, indicating stability in the prevailing reproductive system through time. Yet, our study identified limits by which available theoretical predictions and analytical tools can resolve reproductive system variation using haploid data. There is a need to develop new analytical tools to understand the evolution of sex by expanding our ability to characterize the spatiotemporal variation in reproductive systems across diverse life cycles.

Investigating taxa at varying stages of divergence can shed light on the evolutionary forces that lead to reproductive isolation and eventual speciation. The forces promoting isolation vary in space and time, which makes it difficult to reconstruct the trajectory that resulted in the divergence observed among species today. The red macroalgal genus Plocamium is known worldwide for its cryptic genetic and chemical diversity. Previous work on the genus Plocamium in Antarctica observed two haplotypes along the western Antarctic Peninsula that have been treated as the same species. Using 10 microsatellite loci, we observed that these two haplotypes correspond to two highly divergent, co‐occurring genetic entities in Antarctic Plocamium , which are located within close vicinity of each other at the same sites. The morphology of the reproductive structures, a feature commonly used to identify cryptic species in Plocamium , as well as the timing of reproduction, differed significantly between the two genetic entities. Altogether, this suggests that two Antarctic Plocamium species exist on the western Antarctic Peninsula. We observed evidence for high levels of selfing in both genetic entities, which likely exacerbated the lack of gene flow between them. In addition, we identified concomitant chemodiversity that generates compelling evidence of early evolutionary divergence within one of these entities. This chemodiversity has ecological consequences for its main grazer, which alludes to one putative evolutionary driver of divergence. Antarctic Plocamium spp. provide a promising model system for investigating the eco‐evolutionary forces that initiate and maintain species boundaries.

Life cycles with a prolonged haploid phase are thought to be correlated with greater rates of selfing and asexual reproduction. In red algae, recent population genetic studies have aimed to test this prediction but have mostly focused on marine species with separate sexes. We characterized the reproductive system of the obligately monoicous (i.e., hermaphroditic) freshwater red alga Batrachospermum gelatinosum and predicted that we would find genetic signatures of uniparental reproduction because of its haploid‐diploid life cycle. We sampled 18 sites and genotyped 311 gametophytes with 10 polymorphic microsatellite loci to describe the reproductive system. Genotypic richness was low (<0.5) and pareto β values (describing clonal membership) were <0.7 for most sites. In taxa with separate sexes, these patterns are typically indicative of asexual reproduction. However, the genetic consequences of selfing in monoicous gametophytes are indistinguishable from those caused by asexual processes. Since we sampled gametophytes and have not yet genotyped the chantransia (i.e., the diploid phase), we interpreted low diversity as a signature of intragametophytic selfing. Additionally, to understand the factors that drive selfing, we tested latitude and several other environmental variables, but none was significantly correlated with the genetic variation we observed. Nevertheless, future studies should genotype the chantransia to measure observed heterozygosity among other summary statistics to disentangle the effects of selfing versus asexual reproduction. Together, these data, coupled with further characterization of abiotic factors that influence population genetic patterns, will allow us to test potential drivers of reproductive system evolution.

The relative rates of sexual versus asexual reproduction influence the partitioning of genetic diversity within and among populations. During range expansions, asexual reproduction often facilitates colonization and establishment. The arrival of the green alga Avrainvillea lacerata has caused shifts in habitat structure and community assemblages since its discovery in 1981 offshore of Oʻahu, Hawai‘i. Field observations suggest this species is spreading via vegetative reproduction. To characterize the reproductive system of A. lacerata in Hawai‘i, we developed seven microsatellite loci and genotyped 321 blades collected between 2018 and 2023 from three intertidal sites at Maunalua Bay and ʻEwa Beach. We observed one to four alleles at multiple loci, suggesting A. lacerata is tetraploid. Each site was characterized by high genotypic richness ( R > 0.8). However, clonal rates were also high, suggesting the vegetative spread of A. lacerata plays a significant role. The importance of clonal reproduction for the persistence of A. lacerata in Hawai‘i is consistent with the ecological data collected for this species and observations of other abundant macroalgal invaders in Hawai‘i and other regions of the world. These data demonstrate the necessity for implementing appropriate population genetic methods and provide insights into the biology of this alga that will contribute to future studies on effective management strategies incorporating its reproductive system. This study represents one of the few that investigate green algal population genetic patterns and contributes to our understanding of algal reproductive system evolution.

Temporal population genetic studies have investigated evolutionary processes, but few have characterized the temporal patterns of reproductive system variation. Yet, temporal sampling may improve our understanding of reproductive system evolution through assessing the relative rates of selfing, outcrossing, and clonality. In this study, we focus on the monoicous, haploid-diploid freshwater red alga Batrachospermum gelatinosum. This species has a perennial, microscopic diploid phase (chantransia) that produces an ephemeral, macroscopic haploid phase (gametophyte). Recent work focusing on single time point genotyping suggested high rates of intragametophytic selfing, though there was variation among sites. We expand on this work by genotyping 191 gametophytes from four sites with reproductive system variation at multiple time points within and among years. Intra-annual data suggest shifts in gametophytic genotypes present throughout the gametophytic season. We hypothesize this pattern is likely due to the seasonality of the life cycle and the timing of meiosis among the chantransia. Inter-annual patterns were characterized by consistent genotypic and genetic composition, indicating stability in the prevailing reproductive system through time. Yet, our study identified limits to which available theoretical predictions and analytical tools can resolve reproductive system variation using haploid data. There is a need to develop better tools to understand the evolution of sex by expanding our ability to characterize the spatiotemporal variation in reproductive systems across diverse life cycles.

Pathogen species are experiencing strong joint demographic and selective events, especially when they adapt to a new host, for example through overcoming plant resistance. Stochasticity in the founding event and the associated demographic variations hinder our understanding of the expected evolutionary trajectories and the genetic structure emerging at both neutral and selected loci. What would be the typical genetic signatures of such a rapid adaptation event is not elucidated. Here, we build a demogenetic model to monitor pathogen population dynamics and genetic evolution on two host compartments (susceptible and resistant). We design our model to fit two plant pathogen life cycles, ‘with’ and ‘without’ host alternation. Our aim is to draw a typology of eco-evolutionary dynamics. Using time-series clustering, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to the emergence of genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bot- tleneck on the susceptible host. We pinpoint differences between life cycles with notably more evolutionary rescue ‘with’ host alternation. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes within a few years only. Considering time-series is therefore of utmost importance to accurately decipher pathogen evolution.

The relative rates of sexual versus asexual reproduction influence the partitioning of genetic diversity within and among populations. During range expansions, uniparental reproduction often facilitates colonization and establishment. The arrival of the green alga Avrainvillea lacerata has caused shifts in habitat structure and community assemblages since its discovery in 1981 offshore of west Oahu, Hawaii. Field observations suggest this species is spreading via vegetative reproduction. To characterize the reproductive system of A. lacerata in Hawaii, we developed seven microsatellite loci and genotyped 321 blades collected between 2018 and 2023 from two intertidal sites at Maunalua Bay and 'Ewa Beach. We found one to four alleles at multiple loci, suggesting A. lacerata is tetraploid. Each site was characterized by high genotypic richness (R > 0.8). However, clonal rates were also high at both sites, suggesting vegetative spread of A. lacerata plays a significant role. The importance of clonal reproduction for the persistence of A. lacerata in Hawaii is consistent with the ecological data collected for this species, and observations of other abundant macroalgal invaders in Hawaii and other regions of the world. These data demonstrate the necessity for implementing appropriate population genetic methods and provide insights into the biology of this alga that will contribute to future studies on effective management strategies incorporating its reproductive system. This study represents one of the few investigating green algal population genetic patterns and contributes to our understanding of algal reproductive system evolution.

Reproductive mode, i.e., the proportion of individuals in populations produced by clonality, selfing and outcrossing in populations, determines how hereditary material is transmitted through generations. It shapes genetic diversity and its structure over time and space. Ludwigia grandiflora subsp. hexapetala ( Lgh ) is a partially clonal, polyploid, hermaphroditic, and heteromorphic plant that recently colonized multiple countries worldwide. In western Europe, individuals in this species are either self-incompatible caused by a late-acting self-incompatibility (LSI) system developing long-styled flowers, or self-compatible (SC) developing short-styled flowers. We do not yet know if the LSI system is effective in driving genetic diversity within populations, as previously showed for gametophytic and sporophytic SI systems. In addition, determining the reproductive mode of newly established Lgh populations in Europe will contribute to understanding their ecological and evolutionary roles at the margins of species distribution. However, we still lack of a full approach, including the essential step of unfolding population genetic indices to estimates rates of clonality, selfing and outcrossing in autopolyploids. In this study, we proposed such an approach to measure genetic diversity to assess reproductive modes on 53 LSI and SC populations newly colonizing France and northern Spain, by assessing SNPs on a distinct autotetraploid part of the Lgh genome. SNPs are easily reproducible, adapted for intraspecific genetic studies and allow confident allele dosage to genotype autopolyploid individuals. In turn, such genotyping data made it possible to use recently developed methods for computing and interpreting genetic diversity to assess reproductive mode in each population. We found that populations reproduced mainly clonally but with a high diversity of genotypes along with rates of sexual events up to 40%. We also found evidence for local admixture between LSI and SC populations in a background of genetic structure between pairs of LSI and SC populations that was twice the level found among pairs of LSI populations or pairs of SC populations, arguing that SC and LSI populations may follow distinct expansion dynamics. These observations of sexual events in nearly all populations and of high diversity in clonal lineages imply to integrate their potential adaptation of populations to management plans. We also took advantage of the spatial segregation of LSI and SC populations invading France to characterize the population genetic consequences of an LSI system. LSI and SC populations showed similar rates of clonality but significantly different rates of selfing, as expected considering their breeding system, and despite the small rates of failure in the LSI system. Within the 53 studied populations, the 13 SC-only populations were distinguished by fewer effective alleles, lower observed heterozygosity, and higher inbreeding coefficients, linkage disequilibrium and estimates of selfing than found in LSI populations. These results suggested that genetic structural differences found between LSI and SC populations mainly came from the increased selfing rates in SC populations rather than due to the genome-wide consequences of outcrossing in LSI populations or due to different rates of clonality. The overall maintenance of higher genetic diversity, with the possibility of resorting to clonality, selfing and outcrossing, may explain why LSI populations seem to be more prevalent in all newly expanding populations worldwide. Beyond Lgh , our methodological approach may inspire future studies to assess the reproductive mode of other autopolyploid eukaryote populations, and our results emphasize the necessity to consider the variations of reproductive modes when managing invasive plant species.